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Exploring the Potential of Life-History Key Innovation : Brook Breeding In MEC_1543.fm Page 1453 Tuesday, July 16, 2002 11:31 PM Molecular Ecology (2002) 11, 1453–1463 ExploringBlackwell Science, Ltd the potential of life-history key innovation: brook breeding in the radiation of the Malagasy treefrog genus Boophis M. VENCES,*¶ F. ANDREONE,† F. GLAW,‡ J. KOSUCH,§ A. MEYER,* H.-C. SCHAEFER§ and M. VEITH§ *Department of Biology (Evolutionary Biology), University of Konstanz, 78457 Konstanz, Germany, †Museo Regionale di Scienze Naturali, Laboratory of Vertebrate Taxonomy and Ecology, Via G. Giolitti, 36, 10123 Torino, Italy, ‡Zoologische Staatssammlung München, Münchhausenstrasse 21, 81247 München, Germany, §Institut für Zoologie, Universität Mainz, Saarstraße 21, 55099 Mainz, Germany Abstract The treefrog genus Boophis is one of the most species-rich endemic amphibian groups of Madagascar. It consists of species specialized to breeding in brooks (48 species) and ponds (10 species). We reconstructed the phylogeny of Boophis using 16S ribosomal DNA sequences (558 bp) from 27 species. Brook-breeders were monophyletic and probably derived from an ancestral pond-breeding lineage. Pond-breeders were paraphyletic. The disparity in diversification among pond-breeders and brook-breeders was notable among endemic Malagasy frogs, although it was not significant when considering Boophis alone. Sibling species which have different advertisement calls but are virtually indistinguishable by morphology were common among brook-breeders; genetic divergence between these species was high (modal 8% total pairwise divergence). Substitution rates in brook-breeding species were significantly higher than in pond-breeders. Speciation of pond-breeders may be hindered by their usually more synchronous reproduction and a higher vagility which enhances gene flow, while a higher potential of spatial segregation and speciation may exist along brooks. Keywords: Amphibia, Madagascar, Mantellidae, phylogeny, sibling species Received 28 November 2001; revision received 18 April 2002; accepted 18 April 2002 Recent theoretical and empirical evidence suggests Introduction that rapid diversification processes may in part take place Adaptive radiations have received particular attention as through sympatric rather than allopatric speciation. This sources of organismal diversity. One major topic has been the process is triggered by ecological specialization (Dieckmann exploration of why some lineages gave rise to higher levels & Doebeli 1999) or sexual selection (Higashi et al. 1999; of diversity than others. As an explanation, the influence of key Gavrilets 2000; Boughman 2001). The latter model highlights innovations has often been invoked (Sanderson & Donoghue the importance of optical and other mate recognition 1996). These have been defined as morphological, physiological, mechanisms for speciation (Barraclough et al. 1995). or behavioural traits that enable a lineage to colonize new Treefrogs of the genus Boophis are one of the most adaptive zones and thereby confer the ability to undergo spectacular radiations within the endemic Malagasy family rapid speciation and diversification (Simpson 1953; Liem Mantellidae (Bossuyt & Milinkovitch 2000; Vences & Glaw 1973). 2001). Taking into account recent descriptions, more than 40 nominal and about 18 undescribed Boophis species are attributed to seven phenetic species groups (Blommers- Correspondence: Miguel Vences. ¶Present address: Institute of Biodiversity and Ecosystem Dynamics, Zoological Museum, Schlösser & Blanc 1991; Glaw & Vences 1994, 2000). Among University of Amsterdam, PO Box 94766, 1090 GT Amsterdam, the anurans, the genus Boophis stands out for its large number Netherlands; Fax: + 49 2219417284; E-mail: [email protected] of cryptic sibling species. By morphology alone these are © 2002 Blackwell Science Ltd MEC_1543.fm Page 1454 Tuesday, July 16, 2002 11:31 PM 1454 M. VENCES ET AL. virtually indistinguishable, and they are usually diagnosed Phylogenetic analyses only by their advertisement call or by differences in coloration (Blommers-Schlösser 1979; Glaw & Vences 2000). Phylogenetic analyses were carried out using paup*, version Speciation through call differentiation has been suggested 4b8 (Swofford 2001). Prior to phylogenetic reconstruction, for certain insect groups in which females recognize their we explored which substitution model fitted our sequence mates by species-specific advertisement calls (Henry 1994). data the best. We applied a hierarchical likelihood method Similarly, in Boophis the bioacoustically divergent cryptic to test the goodness-of-fit of nested substitution models, species may also be examples for this type of speciation. If using the program modeltest (Posada & Crandall 1998). this were the case, a low genetic differentiation among many The substitution model estimated as best fitting our data Boophis species would be predicted, as was documented in (see Results) was used to obtain maximum likelihood (ML) other instances of incipient speciation (e.g. Meyer et al. 1990; trees using the heuristic search option, and a random addition- Schliewen et al. 1994; Freeland & Boag 1999; Wilson et al. sequence with 10 replicates. Maximum parsimony (MP) 2000). and neighbour-joining (NJ) trees were also calculated. In this study, we sequenced fragments of the 16S ribosomal In the MP analysis we conducted two heuristic searches, RNA (rRNA) gene from 27 Boophis species to investigate coding each gap (also in multiple gap sequences) either as their phylogenetic relationships, ages and rates of speciation fifth state or as missing character, with branch swapping using among brook and pond-breeding species. We used the the tree bisection-reconnection (TBR) routine. To identify mitochondrial data to test the hypotheses of (i) low genetic multiple islands of equally most parsimonious trees, 100 divergence between sibling species and (ii) reproductive random addition-sequence replicates were performed. Only mode as possible key innovation and mechanism for minimal-length trees were saved and zero-length branches diversification. were collapsed. In the NJ analyses we used LogDet distances, which are robust against possible variation of sequence evolution among lineages (Lockhart et al. 1994). All MP and Material and methods NJ analyses were repeated after exclusion of the hyper- variable region (53 bp). DNA sequencing All available Boophis sequences were included in a first DNA was extracted using QIAmp tissue extraction kits data exploration. To avoid the masking of cladogenetic (Qiagen) from muscle tissue samples preserved in pure patterns in the tests of tree shape and in diversity compar- ethanol. We used the primers 16SA-L (light chain; 5′-CGC isons by inclusion of multiple sequences of the same species, CTG TTT ATC AAA AAC AT-3′) and 16SB-H (heavy chain; we conducted further analyses with a reduced data set of 5′-CCG GTC TGA ACT CAG ATC ACG T-3′) of Palumbi only a single sequence per species. The excluded sequences et al. (1991) to amplify a section [ca. 550 base pairs (bp)] differed by a maximum of only three substitutions from the of the mitochondrial 16S ribosomal RNA gene. We chose included sequences. this gene instead of a more variable marker, such as Two thousand bootstrap replicates (Felsenstein 1985) were cytochrome b or the control region, based on preliminary run in all analyses except ML (only 100 bootstrap replicates data which indicated a high amount of genetic divergence due to computational constraints). The robustness of nodes between Boophis species. Polymerase chain reaction (PCR) was tested by Shimodaira–Hasegawa tests as implemented conditions followed Vences et al. (2000b). PCR products in paup*. Sequences were checked for clock-like behaviour were purified using QIAquick purification kits (Qiagen) using the program tree-puzzle 5.0 (Schmidt et al. 2000). and were sequenced using an automatic DNA sequencer Tests of relative molecular substitution rates (Takezaki (ABI 377). Sequences (see Appendix I for GenBank accession et al. 1995) were conducted using phyltest (Kumar 1996); numbers) were aligned using the computer program of the different substitution models implemented in this sequence navigator 2.0 (Applied Biosystems), taking program, we used Jukes–Cantor distances, uncorrected secondary structures into account (Kjer 1995). The alignment P-distances of transversion only, Kimura two-parameter needed single gaps at four positions, double gaps at two distances, and Kimura two-parameter distances of trans- positions, and three or four consecutive gaps at two versions only. additional positions. Of the latter two cases, one was due to insertions in only four species, while the second was within Tests of diversification rate and tree imbalance a hypervariable region of 53 bp (positions 257–309 of the alignment). Although disparities in species numbers among lineages In addition to our own data we also re-analysed the five may seem obvious, the differences are not significant in many Boophis sequences from the work of Richards et al. (2000) cases. Under a Markovian model of cladogenesis a stochastic who studied higher-level relationships in a more inclusive difference in initial rates can lead to a much higher diversity sample of Malagasy frogs. in one of the lineages (Slowinski & Guyer 1989). Careful © 2002 Blackwell Science Ltd, Molecular Ecology, 11, 1453–1463 MEC_1543.fm Page 1455 Tuesday, July 16, 2002 11:31 PM RADIATION OF TREEFROGS IN MADAGASCAR 1455 examination of the initial data is therefore needed to assess (Sanderson 1997).
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